Comparison of molecular and serological isolation methods to identify pigeons suspected of having avian tuberculosis
Subject Areas :
Veterinary Clinical Pathology
mahsa lari baghal
1
,
Mansour Mayahi
2
,
Zahra Boroomand
3
,
Nader Mosavari
4
1 - Specialist in Poultry Health and Diseases, Faculty of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran.
2 - Professor of Clinical Sciences, Faculty of Veterinary Medicine, Shahid Chamran University of Ahvaz; Ahvaz, Iran.
3 - Professor of Clinical Sciences, Faculty of Veterinary Medicine, Shahid Chamran University of Ahvaz; Ahvaz, Iran.
4 - Reference Laboratory, Razi Vaccine and Serum Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran.
Received: 2021-11-16
Accepted : 2022-03-13
Published : 2022-01-21
Keywords:
isolation,
Mycobacterium,
pigeon,
Serology,
Molecular identification,
Abstract :
Tuberculosis is one of the oldest infectious zoonotic diseases. The importance of avian tuberculosis and the growing risk of the disease in human societies have provided a double incentive for rapid diagnosis of the disease. Mycobacterium avium subsp. avium is the most important cause of disease in poultry. Sampling for the present research was done during 2018-2019. Based on clinical signs and poor physical condition, 101 pigeons suspected of having tuberculosis were selected from different herds. First, blood samples were taken from pigeons for serum preparation. Then pigeons were euthanized and necropsy was performed and tissue samples were taken for culture and molecular tests. The samples were cultured in three specific media: Lunstein-Johnson with glycerin, Lunstein-Johnson with pyruvate and Heroldegg. Molecular analysis of samples was conducted using 16S rRNA, IS1245, and IS901 primers. Serum samples were analyzed for antibodies against Mycobacterium avium using a specifically designed ELISA system. Based on culture and molecular identification, 39 isolates from Mycobacterium avium subsp. avium were isolated. Contamination of 13 pigeons with Mycobacterium avium subsp. avium was detected using the specifically designed ELISA system. According to the results, the sensitivity of the culture and PCR methods was higher than the specifically designed ELISA system. However, due to the significant relationship between these three methods, it seems that the ELISA system can be used to screen flocks in the early stages of the disease.
References:
Asadollahi, K., Mosavari, N. and Mayahi, M. (2015). Genotyping of Mycobacterium avium subsp. avium isolates from naturally infected lofts of domestic pigeons in Ahvaz by IS901 RFLP. Iranian Journal of Microbiology, 7(5): 260-264.
Barberis, I., Bragazzi, N.L., Galluzzo, L. and Martini, M. (2017). The history of tuberculosis: from the first historical records to the isolation of Koch's bacillus, Journal of Preventive Medicine and Hygiene, 58(1): E9-E12.
Boulfion, M. (2009). Molecular Identification of Mycobacteria Isolated from Pigeons Submitted to Razi Institute. Postgraduate Thesis from Azad University Research Science Branch, Tehran, No. 5469. [In Persian]
Christal, G.P. (2013). Implications of Mycobacterium in Clinical Disorders. Chapter 28, pp: 681- 689.
Cromie, R.L., Ash, N.J., Brown, M.J. and Stanford, J.L. (2000). Avian immune Responses to Mycobacterium avium: the wildfowl example. Developmental & Comparative Immunology, 24(2-3): 169-185.
Cromie, R.L., Brown, M.J., Forbes, N.A., Morgan, J. and Stanford, J.L. (1993). A comparison and evaluation of techniques for diagnosis of avian tuberculosis in wildfowl. Avian Pathology, 22(3): 617- 630.
Dhama, K., Mahendran, M., Tiwari, R., Dayal Singh, S., Kumar, D., Sing, S., et al. (2011). Tuberculosis in birds: Insight into the Mycobacterium avium infections. Veterinary Medicine International, 712369: 1-14.
Dvorska, L., Bull, T.J., Bartos, M., Matlova, L., Svastova, P., Weston, RT., et al. (2003). A standardized restriction fragment length polymorphism (RFLP) method for typing Mycobacterium avium isolates links IS901 with virulence for birds. Journal of Microbiological Methods, 55(1): 11-27.
Friend, M., Robert, G., McLean, and Deín, FJ. (2001). Disease emergence in birds: challenges for the twenty-first century. The Auk, 118(2): 290-303.
Fulton, RM. and Sanchez, S. (2020). Tuberculosis. In: Other Bacterial Diseases, Tuberculosis. In David E.S. editor. Disease of Poultry. 14th ed., Blackwel Publishing, pp: 1033-1043.
Fulton, R.M. and Thoen, C.O. (2003). Tuberculosis, In: Saif, Y.M., Barnes, H.J., Glisson, J.R., Fadly, F.M., Mc Dougald, L.R. and Swayne, D.E. editors. Diseases of Poultry. Iowa State University Press, Ames, IA, USA, pp: 836-844.
Ghadiri, K., Izadi, B., Afsharian, M., Rezaei, M. and Namdari, S. (2006). Evaluation of diagnostic value of serological tests (IgA, IgG, IgM) in the diagnosis of tuberculosis in Kermanshah in 2003-2005. Journal of Infectious and Tropical Diseases affiliated to the Association of Infectious and Tropical Diseases Specialists, 35(11): 55-58. [In Persian]
Gholoobi , A., Masoudi-Kazemabad, A., Meshkat , M. and Meshkat, Z. (2014). Comparison of Culture and PCR Methods for Diagnosis of Mycobacterium tuberculosis in Different Clinical Specimens. Jundishapur Journal of Microbiology, 7(2): e8939.
Guerrero, C., Bernasconi, C., Burki, D., Bodmer T. and Telenti, A. (1995). A novel insertion element from Mycobacterium avium, IS1245, is a specific target for analysis of strain relatedness. Journal of Clinical Microbiology, 33(2): 303-304.
Hawkey, C., Kock, RA., Henderson, GM. and Cindery, RN. (1990). Hematological changes in domestic fowl (Gallus gallus) and cranes (Gruiformes) with Mycobacterium avium infection. Avian Pathology, 19: 223-234.
Huard, R.C., Lazzarini, L.C., Butler, W.R. and Van soolingen, D. (2003). PCR-based method to differentiate the subspecies of the Mycobacterium tuberculosis complex on the basis of genomic deletions. Journal of Clinical Microbiology, 41(4): 1637-1650.
Izadi, H., Sohrabi, N., Tebyanian, M., Musouri, N. and Mahdavi, M. (2015). Evaluation of serum levels of specific antibodies against recombinant ESAT-6 antigen in patients with tuberculosis compared with healthy individuals. Journal of Fasa University of Medical Sciences. 4(6): 474-480. [In Persian]
Jabbarzadeh, I. and Seifi, M. (2010). Rapid identification of different species of Mycobacterium in tuberculosis. Journal of Veterinary Clinical Research. 1(2): 5-13. [In Persian]
Jorgensen, J.P. (1978). Serological investigation of strains of Mycobacterium avium and Mycobacterium intracellulare isolated from animal and non-animal sources. Nordisk Veterinary Medicine, 30(4-5): 150-162.
Kaevska, M., Slana, I., Kralik, P. and Pavlik, I. (2010). Examination of Mycobacterium avium subsp. avium distribution in naturally infected hens by culture and triplex quantitative real time PCR. Veterinarni Medicina, 55(7): 325-330.
Kriz, P., Slana, I., Mrlik, V., Moravkova, M., Kralova, A., Krizova, K., et al. (2010). Mycobacterium avium subsp. avium in domestic pigeons (Columba livia f. domestica) diagnosed by direct conventional multiplex PCR: a case report. Veterinarni Medicina, 55(2): 87-90.
Kunze, Z.M., Wall, S., Appelberg, R., Silva, M.T., Portales, F. and Mcfadden, J.J. (1991). IS901, a new member of a widespread class of atypical insertion sequences, is associated with pathogenicity in Mycobacterium avium. Molecular Microbiology, 5(9): 226-227.
Mayahi, M., Mosavari, N., Esmaeilzadeh, S. and Asadollahi, P.K. (2013). Comparison of four different culture media for growth of Mycobacterium avium subsp. avium isolated from naturally infected lofts of domestic pigeons. Iranian Journal of Microbiology, 5(4): 379-382.
Movassaghi, A.R., Haghshenas, K.H. and Farzin, H.R. (2010). Granulomatous dermatitis caused by Mycobacterium Spp. in pigeons (first report). 4th Iranian Congress of Clinical Microbiology, pp: 9-11.
Nouri, M., Azarabad, H. and Moeini Jazani, M. (2012). Cutaneous tuberculosis, coccidiosis, cestode infection, and trichoepithelioma in a columba pigeon (Columba livia). Second National Congress of Veterinary Laboratory Sciences. pp: 251. [In Persian]
O’Brien, A., Clare W., Clarke, J.B., Hayton, A., Watt, N.J. and Harkiss, G.D. (2017). Serological Analysis of Tuberculosis in Goats by Use of the Enferplex Caprine TB Multiplex Test. Clinical and Vaccine Immunology, 24(2): e00516-518.
Pavlas, M., Michalska, A. and Hunady, M. (1992). Diagnosis of avian tuberculosis-mycobacteriosis by rapid agglutination. Acta Veterinaria Brno, 62(1): 63-69.
Pesek, L. (1998). Zoonotic Diseases (Birds -Humans): Avian Tuberculosis, Bird to Human Transmission. Pet Bird Magazine.
Phalen, D.N., Grimes J.E. and Phalen, S.W. (1995). Serologic diagnosis of mycobacterial infections in birds (a preliminary report). Proceeding of the Association of Avian Veterinarians, 40: 67-73.
Sattar, A., Zakaria, Z., Abu, J., Saleha A, A. and Gabriel, RP. (2021). Isolation of Mycobacterium avium and other nontuberculous mycobacteria in chickens and captive birds in peninsular Malaysia. BMC Veterinary Research, 17(13): 1-13.
Shitaye, J.E., Matlova, L., Horvathova, A., Moravkova, M., Dvorska-Bartosova, L., Trcka, I., et al. (2008a). Diagnostic testing of different stages of avian tuberculosis in naturally infected hens (Gallus domesticus) by the tuberculin skin and rapid agglutination tests, faecal and egg examinations. Veterinarni Medicina, 53(2): 101-110.
Shitaye, J.E., Matlova, L., Horvathova, A., Morvathova, M., Dvorska-Bartosova, L., Treml, F., et al. (2008b). Mycobacterium avium subsp. avium distribution studied in a naturally infected hen flock and in the environment by culture, serotyping and IS901 RFLP methods. Veterinary Microbiology, 127(1-2): 155-164.
Singhla, T., Boonyayatra, S., Chulakasian, S., Lukkana, M., Alvarez, J., Sreevatsan S., et al. (2019). Determination of the sensitivity and specificity of bovine tuberculosis screening tests in dairy herds in Thailand using a Bayesian approach. BMC Veterinary Research, 15(149): 1-7.
Taroudizadeh, Y. and Imani Fouladi, A.A. (2012). Investigation of underlying and environmental factors causing tuberculosis. Scientific Journal of the Medical System Organization of the Islamic Republic of Iran. 30(4): 335-340. [In Persian]
Tell, L.A., Woods, L. and Cromie, R.L. (2001). Mycobacteriosis in birds. “Avian tuberculosis in birds”. Review Science and Technology office Internationale des Epizooties, 20(1): 180-203.
Thoen, C.O., Armbrust, A.L. and Hopkins, M.P. (1979): Enzyme- linked immunosorbent assay for detecting antibodies in swine infected with Mycobacterium avium. American Journal of Veterinary Research, 40(8): 1096-1099.
Van der Heyden, N. (1997). Mycobacterial infections: new strategies in the treatment of avian mycobacteriosis. Seminars in Avian Exotic Pet Medicine, 6(1): 25-33.
Van Soolingen, D., de Haas, P.E.W. and Kremer, K. (2002). Restriction Fragment Length Polymorphism (RFLP) Typing of Mycobacteria. National Institute of Public Health and the Environment, Bilthoven, 54: 165-203.
Velayati, A.A. (1977). Tuberculosis Disease. Vol. 1, 1st ed., University Publication Center: 1-908. [In Persian]
Wobeser, G.A. (1997). Tuberculosis. Diseases of Wild Waterfowl. 2nd, New York, N.Y. Plenum Press, pp: 71-75.
Wood, P.R., Corner, L.A., Rothel, J.S., Ripper, J.L., Fifis, T., McCormick, B.S., et al. (1992). A field evaluation of serological and cellular diagnostic tests for bovine tuberculosis. Veterinary Microbiology, 31(1): 71-79.
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Asadollahi, K., Mosavari, N. and Mayahi, M. (2015). Genotyping of Mycobacterium avium subsp. avium isolates from naturally infected lofts of domestic pigeons in Ahvaz by IS901 RFLP. Iranian Journal of Microbiology, 7(5): 260-264.
Barberis, I., Bragazzi, N.L., Galluzzo, L. and Martini, M. (2017). The history of tuberculosis: from the first historical records to the isolation of Koch's bacillus, Journal of Preventive Medicine and Hygiene, 58(1): E9-E12.
Boulfion, M. (2009). Molecular Identification of Mycobacteria Isolated from Pigeons Submitted to Razi Institute. Postgraduate Thesis from Azad University Research Science Branch, Tehran, No. 5469. [In Persian]
Christal, G.P. (2013). Implications of Mycobacterium in Clinical Disorders. Chapter 28, pp: 681- 689.
Cromie, R.L., Ash, N.J., Brown, M.J. and Stanford, J.L. (2000). Avian immune Responses to Mycobacterium avium: the wildfowl example. Developmental & Comparative Immunology, 24(2-3): 169-185.
Cromie, R.L., Brown, M.J., Forbes, N.A., Morgan, J. and Stanford, J.L. (1993). A comparison and evaluation of techniques for diagnosis of avian tuberculosis in wildfowl. Avian Pathology, 22(3): 617- 630.
Dhama, K., Mahendran, M., Tiwari, R., Dayal Singh, S., Kumar, D., Sing, S., et al. (2011). Tuberculosis in birds: Insight into the Mycobacterium avium infections. Veterinary Medicine International, 712369: 1-14.
Dvorska, L., Bull, T.J., Bartos, M., Matlova, L., Svastova, P., Weston, RT., et al. (2003). A standardized restriction fragment length polymorphism (RFLP) method for typing Mycobacterium avium isolates links IS901 with virulence for birds. Journal of Microbiological Methods, 55(1): 11-27.
Friend, M., Robert, G., McLean, and Deín, FJ. (2001). Disease emergence in birds: challenges for the twenty-first century. The Auk, 118(2): 290-303.
Fulton, RM. and Sanchez, S. (2020). Tuberculosis. In: Other Bacterial Diseases, Tuberculosis. In David E.S. editor. Disease of Poultry. 14th ed., Blackwel Publishing, pp: 1033-1043.
Fulton, R.M. and Thoen, C.O. (2003). Tuberculosis, In: Saif, Y.M., Barnes, H.J., Glisson, J.R., Fadly, F.M., Mc Dougald, L.R. and Swayne, D.E. editors. Diseases of Poultry. Iowa State University Press, Ames, IA, USA, pp: 836-844.
Ghadiri, K., Izadi, B., Afsharian, M., Rezaei, M. and Namdari, S. (2006). Evaluation of diagnostic value of serological tests (IgA, IgG, IgM) in the diagnosis of tuberculosis in Kermanshah in 2003-2005. Journal of Infectious and Tropical Diseases affiliated to the Association of Infectious and Tropical Diseases Specialists, 35(11): 55-58. [In Persian]
Gholoobi , A., Masoudi-Kazemabad, A., Meshkat , M. and Meshkat, Z. (2014). Comparison of Culture and PCR Methods for Diagnosis of Mycobacterium tuberculosis in Different Clinical Specimens. Jundishapur Journal of Microbiology, 7(2): e8939.
Guerrero, C., Bernasconi, C., Burki, D., Bodmer T. and Telenti, A. (1995). A novel insertion element from Mycobacterium avium, IS1245, is a specific target for analysis of strain relatedness. Journal of Clinical Microbiology, 33(2): 303-304.
Hawkey, C., Kock, RA., Henderson, GM. and Cindery, RN. (1990). Hematological changes in domestic fowl (Gallus gallus) and cranes (Gruiformes) with Mycobacterium avium infection. Avian Pathology, 19: 223-234.
Huard, R.C., Lazzarini, L.C., Butler, W.R. and Van soolingen, D. (2003). PCR-based method to differentiate the subspecies of the Mycobacterium tuberculosis complex on the basis of genomic deletions. Journal of Clinical Microbiology, 41(4): 1637-1650.
Izadi, H., Sohrabi, N., Tebyanian, M., Musouri, N. and Mahdavi, M. (2015). Evaluation of serum levels of specific antibodies against recombinant ESAT-6 antigen in patients with tuberculosis compared with healthy individuals. Journal of Fasa University of Medical Sciences. 4(6): 474-480. [In Persian]
Jabbarzadeh, I. and Seifi, M. (2010). Rapid identification of different species of Mycobacterium in tuberculosis. Journal of Veterinary Clinical Research. 1(2): 5-13. [In Persian]
Jorgensen, J.P. (1978). Serological investigation of strains of Mycobacterium avium and Mycobacterium intracellulare isolated from animal and non-animal sources. Nordisk Veterinary Medicine, 30(4-5): 150-162.
Kaevska, M., Slana, I., Kralik, P. and Pavlik, I. (2010). Examination of Mycobacterium avium subsp. avium distribution in naturally infected hens by culture and triplex quantitative real time PCR. Veterinarni Medicina, 55(7): 325-330.
Kriz, P., Slana, I., Mrlik, V., Moravkova, M., Kralova, A., Krizova, K., et al. (2010). Mycobacterium avium subsp. avium in domestic pigeons (Columba livia f. domestica) diagnosed by direct conventional multiplex PCR: a case report. Veterinarni Medicina, 55(2): 87-90.
Kunze, Z.M., Wall, S., Appelberg, R., Silva, M.T., Portales, F. and Mcfadden, J.J. (1991). IS901, a new member of a widespread class of atypical insertion sequences, is associated with pathogenicity in Mycobacterium avium. Molecular Microbiology, 5(9): 226-227.
Mayahi, M., Mosavari, N., Esmaeilzadeh, S. and Asadollahi, P.K. (2013). Comparison of four different culture media for growth of Mycobacterium avium subsp. avium isolated from naturally infected lofts of domestic pigeons. Iranian Journal of Microbiology, 5(4): 379-382.
Movassaghi, A.R., Haghshenas, K.H. and Farzin, H.R. (2010). Granulomatous dermatitis caused by Mycobacterium Spp. in pigeons (first report). 4th Iranian Congress of Clinical Microbiology, pp: 9-11.
Nouri, M., Azarabad, H. and Moeini Jazani, M. (2012). Cutaneous tuberculosis, coccidiosis, cestode infection, and trichoepithelioma in a columba pigeon (Columba livia). Second National Congress of Veterinary Laboratory Sciences. pp: 251. [In Persian]
O’Brien, A., Clare W., Clarke, J.B., Hayton, A., Watt, N.J. and Harkiss, G.D. (2017). Serological Analysis of Tuberculosis in Goats by Use of the Enferplex Caprine TB Multiplex Test. Clinical and Vaccine Immunology, 24(2): e00516-518.
Pavlas, M., Michalska, A. and Hunady, M. (1992). Diagnosis of avian tuberculosis-mycobacteriosis by rapid agglutination. Acta Veterinaria Brno, 62(1): 63-69.
Pesek, L. (1998). Zoonotic Diseases (Birds -Humans): Avian Tuberculosis, Bird to Human Transmission. Pet Bird Magazine.
Phalen, D.N., Grimes J.E. and Phalen, S.W. (1995). Serologic diagnosis of mycobacterial infections in birds (a preliminary report). Proceeding of the Association of Avian Veterinarians, 40: 67-73.
Sattar, A., Zakaria, Z., Abu, J., Saleha A, A. and Gabriel, RP. (2021). Isolation of Mycobacterium avium and other nontuberculous mycobacteria in chickens and captive birds in peninsular Malaysia. BMC Veterinary Research, 17(13): 1-13.
Shitaye, J.E., Matlova, L., Horvathova, A., Moravkova, M., Dvorska-Bartosova, L., Trcka, I., et al. (2008a). Diagnostic testing of different stages of avian tuberculosis in naturally infected hens (Gallus domesticus) by the tuberculin skin and rapid agglutination tests, faecal and egg examinations. Veterinarni Medicina, 53(2): 101-110.
Shitaye, J.E., Matlova, L., Horvathova, A., Morvathova, M., Dvorska-Bartosova, L., Treml, F., et al. (2008b). Mycobacterium avium subsp. avium distribution studied in a naturally infected hen flock and in the environment by culture, serotyping and IS901 RFLP methods. Veterinary Microbiology, 127(1-2): 155-164.
Singhla, T., Boonyayatra, S., Chulakasian, S., Lukkana, M., Alvarez, J., Sreevatsan S., et al. (2019). Determination of the sensitivity and specificity of bovine tuberculosis screening tests in dairy herds in Thailand using a Bayesian approach. BMC Veterinary Research, 15(149): 1-7.
Taroudizadeh, Y. and Imani Fouladi, A.A. (2012). Investigation of underlying and environmental factors causing tuberculosis. Scientific Journal of the Medical System Organization of the Islamic Republic of Iran. 30(4): 335-340. [In Persian]
Tell, L.A., Woods, L. and Cromie, R.L. (2001). Mycobacteriosis in birds. “Avian tuberculosis in birds”. Review Science and Technology office Internationale des Epizooties, 20(1): 180-203.
Thoen, C.O., Armbrust, A.L. and Hopkins, M.P. (1979): Enzyme- linked immunosorbent assay for detecting antibodies in swine infected with Mycobacterium avium. American Journal of Veterinary Research, 40(8): 1096-1099.
Van der Heyden, N. (1997). Mycobacterial infections: new strategies in the treatment of avian mycobacteriosis. Seminars in Avian Exotic Pet Medicine, 6(1): 25-33.
Van Soolingen, D., de Haas, P.E.W. and Kremer, K. (2002). Restriction Fragment Length Polymorphism (RFLP) Typing of Mycobacteria. National Institute of Public Health and the Environment, Bilthoven, 54: 165-203.
Velayati, A.A. (1977). Tuberculosis Disease. Vol. 1, 1st ed., University Publication Center: 1-908. [In Persian]
Wobeser, G.A. (1997). Tuberculosis. Diseases of Wild Waterfowl. 2nd, New York, N.Y. Plenum Press, pp: 71-75.
Wood, P.R., Corner, L.A., Rothel, J.S., Ripper, J.L., Fifis, T., McCormick, B.S., et al. (1992). A field evaluation of serological and cellular diagnostic tests for bovine tuberculosis. Veterinary Microbiology, 31(1): 71-79.